Adaptive defence-related changes in the metabolome of Sorghum bicolor cells in response to lipopolysaccharides of the pathogen Burkholderia andropogonis.
Journal
Scientific reports
ISSN: 2045-2322
Titre abrégé: Sci Rep
Pays: England
ID NLM: 101563288
Informations de publication
Date de publication:
06 05 2020
06 05 2020
Historique:
received:
10
10
2019
accepted:
06
04
2020
entrez:
8
5
2020
pubmed:
8
5
2020
medline:
2
12
2020
Statut:
epublish
Résumé
Plant cell suspension culture systems are valuable for the study of complex biological systems such as inducible defence responses and aspects of plant innate immunity. Perturbations to the cellular metabolome can be investigated using metabolomic approaches in order to reveal the underlying metabolic mechanism of cellular responses. Lipopolysaccharides from the sorghum pathogen, Burkholderia andropogonis (LPS
Identifiants
pubmed: 32376849
doi: 10.1038/s41598-020-64186-y
pii: 10.1038/s41598-020-64186-y
pmc: PMC7203242
doi:
Substances chimiques
Lipopolysaccharides
0
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
7626Références
Ranf, S. Pattern recognition receptors – versatile genetic tools for engineering broad-spectrum disease resistance in crops. Agronomy 8, 134, https://doi.org/10.3390/agronomy8080134 (2018).
doi: 10.3390/agronomy8080134
Mareya, C. R. et al. Untargeted metabolomics reveal defensome-related metabolic reprogramming in Sorghum bicolor against infection by Burkholderia andropogonis. Metabolites, 9, https://doi.org/10.3390/metabo9010008 (2019).
Andolfo, G. & Ercolano, M.R. Plant innate immunity multicomponent model. Front. Plant Sci. 6, https://doi.org/10.3389/fpls.2015.00987 (2015).
Sanabria, N. M., Huang, J.-C. & Dubery, I. A. Self/nonself perception in plants in innate immunity and defense. Self/ Nonself 1, 40–54 (2010).
pubmed: 21559176
pmcid: 3091600
Choi, H.W. & Klessig, D.F. DAMPs, MAMPs and NAMPs in plant innate immunity. BMC Plant Biol. 16, https://doi.org/10.1186/s12870-016-0921-2. (2016).
Ranf, S. Immune sensing of lipopolysaccharide in plants and animals: same but different. PLoS Pathog. 12(6), e1005596, https://doi.org/10.1371/journal.ppat.1005596 (2016).
doi: 10.1371/journal.ppat.1005596
pubmed: 27281177
pmcid: 4900518
Newman, M. A., von Roepenack, E., Daniels, M. & Dow, M. Lipopolysaccharides and plant responses to phytopathogenic bacteria. Mol. Plant Pathol. 1, 25–31 (2000).
pubmed: 20572947
Kutschera, A. & Ranf, S. The multifaceted functions of lipopolysaccharide in plant-bacteria interactions. Biochimie 159, 93–98 (2019).
pubmed: 30077817
Di Lorenzo, F. et al. Lipopolysaccharides as microbe-associated molecular patterns: A structural perspective in Carbohydrates in drug design and discovery, (eds. Jimenez-Barbero, J., Canada, F.J. & Martín-Santamaría, S.) 38–63 (RSC Publishing, London, 2015).
De Castro., C. et al. Structural identification of the O-antigen fraction from the lipopolysaccharide of the Burkholderia ambifaria strain 19182. Carbohydr. Res. 379, 95–99 (2013).
pubmed: 23886988
Madala, N. E., Molinaro, A. & Dubery, I. A. Distinct carbohydrate and lipid-based molecular patterns within lipopolysaccharides from Burkholderia cepacia contribute to defense-associated differential gene expression in Arabidopsis thaliana. Innate Immun. 18, 140–154 (2012).
pubmed: 21733976
Di Lorenzo, F. The lipopolysaccharide lipid A structure from the marine sponge-associated bacterium Pseudoalteromonas sp. 2A. Anton. van Leeuwenhoek. J. Microbiol. 110, 1401–1412 (2017).
Sanabria, N. M. & Dubery, I. A. Differential display profiling of the Nicotiana response to LPS reveals elements of plant basal resistance. Biochem. Biophys. Res. Commun. 344, 1001–1007 (2006).
pubmed: 16643858
Madala, N. E., Leone, M. R., Molinaro, A. & Dubery, I. A. Deciphering the structural and biological properties of the lipid A moiety of lipopolysaccharides from Burkholderia cepacia strain ASP B 2D, in Arabidopsis thaliana. Glycobiology 21, 184–194 (2011).
pubmed: 20943675
Di Lorenzo, F. et al. The Lipid A from Rhodopseudomonas palustris strain BisA53 LPS possesses a unique structure and low immunostimulant properties. Chem. Euro. Journ. 23, 1–12 (2016).
Newman, M.A., Sundelin, T., Nielsen, J.T. & Erbs, G. MAMP (microbe-associated molecular pattern) triggered immunity in plants. Front. Plant Sci. 4, 10.3389/fpls.2013.00139 PMID: 23720666 (2013).
Ranf, S. et al. A lectin S-domain receptor kinase mediates lipopolysaccharide sensing in Arabidopsis thaliana Nat. Immunol. 10, 1038/ni.3124 (2015).
James, J. T., Tugizimana, F., Steenkamp, P. A. & Dubery, I. A. Metabolomic analysis of methyl jasmonate-induced triterpenoid production in the medicinal herb Centella asiatica (L.) urban. Molecules 18, 4267–4281 (2013).
pubmed: 23579994
pmcid: 6270148
Djami-Tchatchou, A.T., Ncube, E.N., Steenkamp, P.A. & Dubery I.A. Similar, but different: Structurally related azelaic acid and hexanoic acid trigger differential metabolomic and transcriptomic responses in tobacco cells. BMC Plant Biol. 17, https://doi.org/10.1186/s12870-017-1157-5 (2017).
Tugizimana, F., Steenkamp, P. A., Piater, L. A. & Dubery, I. A. Ergosterol-induced sesquiterpenoid synthesis in tobacco cells. Molecules 17, 1698–1715 (2012).
pubmed: 22322447
pmcid: 6268458
Finnegan, T., Steenkamp, P.A., Piater, L.A. & Dubery, I.A. The lipopolysaccharide-induced metabolome signature in Arabidopsis thaliana reveals dynamic reprogramming of phytoalexin and phytoanticipin pathways. PLoS One, 11, https://doi.org/10.1371/journal.pone.0163572 (2016).
Mhlongo, M.I., Piater, L.A., Madala, N.E., Steenkamp, P.A & Dubery, I.A. Phenylpropanoid defences in Nicotiana tabacum cells: Overlapping metabolomes indicate common aspects to priming responses induced by lipopolysaccharides, chitosan and flagellin-22. PLoS One, 11, https://doi.org/10.1371/journal.pone.0151350 (2016).
Tugizimana, F., Djami-Tchatchou, A.T., Steenkamp, P.A., Piater, L.A. & Dubery, I.A. Metabolomic analysis of defense-related reprogramming in Sorghum bicolor in response to Colletotrichum sublineolum infection reveals a functional metabolic web of phenylpropanoid and flavonoid pathways. Front. Plant Sci. 9, https://doi.org/10.3389/fpls.2018.01840 (2019).
Di Lorenzo, F. et al. Chemistry and biology of the potent endotoxin from a Burkholderia dolosa clinical isolate from a cystic fibrosis patient. ChemBioChem. 14, 1105–1115 (2013).
pubmed: 23733445
Tugizimana, F., Piater, L.A. & Dubery, I.A. Plant metabolomics: A new frontier in phytochemical analysis. S. Afr. J. Sci. 109, https://doi.org/10.1590/sajs.2013/20120005 (2013).
Jolliffe, I.T., & Cadima J. Principal component analysis: a review and recent developments. Philos Trans. Roy. Soc. A. 374, https://doi.org/10.1098/rsta.2015.0202 (2016).
Tugizimana, F., Steenkamp, P.A., Piater, L.A & Dubery, I.A. Multi-platform metabolomic analyses of ergosterol- induced dynamic changes in Nicotiana tabacum cells. PLoS One, 9, https://doi.org/10.1371/journal.pone.0087846 (2014).
Tugizimana, F., Ncube, E. N., Steenkamp, P. A. & Dubery, I. A. Metabolomics-derived insights into the manipulation of terpenoid synthesis in Centella asiatica cells by methyl jasmonate. Plant Biotechnol. Rep. 9, 125–136 (2015).
Tugizimana, F., Steenkamp, P. A., Piater, L. A. & Dubery, I. A. Mass spectrometry in untargeted liquid chromatography / mass spectrometry metabolomics: Electrospray ionisation parameters and global coverage of the metabolome. Rapid Commun. Mass Spectrom. 32, 121–132 (2018).
pubmed: 28990281
Sumner, L. W. et al. Proposed minimum reporting standards for chemical analysis: Chemical Analysis Working Group (CAWG) Metabolomics Standards Initiative (MSI). Metabolomics 3, 211–221 (2007).
pubmed: 24039616
pmcid: 3772505
Lerouge, I. & Vanderleyden, J. O-Antigen structural variation: mechanisms and possible roles in animal/plant-microbe interactions. FEMS Microbiol. Rev. 26, 17–47 (2001).
Seydel, U., Schromm, A. B., Blunck, R. & Brandenburg, K. Chemical structure, molecular conformation and bioactivity of endotoxins. Chem Immunol. 74, 5–24 (2000).
pubmed: 10608079
Zdorovenko, E. L. et al. Structure of the O-polysaccharide of Azorhizobium caulinodans HAMBI 216; identification of 3-C-methyl-D-rhamnose as a component of bacterial polysaccharides. Carbohydr. Res. 358, 106–9, https://doi.org/10.1016/j.carres.2012.06.012 (2012).
doi: 10.1016/j.carres.2012.06.012
pubmed: 22819626
Molinaro, A. et al. Chemistry of Lipid A: At the heart of innate immunity. Chem. Eur. J. 20, 1–21 (2014).
Salzman, R. A. et al. Transcriptional profiling of sorghum induced by methyl jasmonate, salicylic acid, and aminocyclopropane carboxylic acid reveals cooperative regulation and novel gene responses. Plant Physiol. 138, 352–368 (2005).
pubmed: 15863699
pmcid: 1104189
Taheri, P. & Tarighi, S. Riboflavin induces resistance in rice against Rhizoctonia solani via jasmonate-mediated priming of phenylpropanoid pathway. J Plant Physiol. 167, 201–208 (2010).
pubmed: 19729221
Petrussa, E. et al. Plant flavonoids-biosynthesis, transport and involvement in stress responses. Int. J. Mol. Sci. 14, 14950–14973 (2013).
pubmed: 23867610
pmcid: 3742282
Zhao, J., Davis, L. C. & Verpoorte, R. Elicitor signal transduction leading to production of plant secondary metabolites. Biotechnol. Adv. 23, 283–333 (2005).
pubmed: 15848039
Poloni, A. & Schirawski, J. Red card for pathogens: Phytoalexins in sorghum and maize. Molecules 19, 9114–9133 (2014).
pubmed: 24983861
pmcid: 6271655
Lukaszuk, E. & Ciereszko, I. Plant responses to wounding stress. In: Biological diversity – from cell to ecosystem (ed. Laska, G.) 73-85 (Polish Botanical Society, 2012). ISBN 978-83-62069-28-6.
Chamarthi, S. K. et al. Identification of fusarium head blight resistance related metabolites specific to doubled-haploid lines in barley. Eur. J. Plant Pathol. 138, 67–78 (2014).
Eckardt, N. A. Oxylipins signaling in plant stress responses. Plant Cell 20, 495–497 (2008).
pubmed: 18359852
pmcid: 2329930
Gao, Q.M., Zhu, S., Kachroo, P. & Kachroo, A. Signal regulators of systemic acquired resistance. Front. Plant Sci. 6, https://doi.org/10.3389/fpls.2015.00228 (2015).
Shah, J., Zeier, J. & Cameron, R.K. Long-distance communication and signal amplification in systemic acquired resistance. Front. Plant Sci. 4, https://doi.org/10.3389/fpls.2013.00030 (2013).
Shine, M. B., Xiao, X., Kachroo, P. & Kachroo, A. Signaling mechanisms underlying systemic acquired resistance to microbial pathogens. Plant Sci. 279, 81–86, https://doi.org/10.1016/j.plantsci.2018.01.001 (2018).
doi: 10.1016/j.plantsci.2018.01.001
pubmed: 30709496
Huang, J.-C., Piater, L. A. & Dubery, I. A. Identification and characterization of a differentially expressed NAC transcription factor gene in MAMP-treated. Arabidopsis thaliana. Physiol. Mol. Plant Pathol. 80, 19–27 (2012).
Denancé, N., Sánchez-Vallet, A., Goffner, D. & Molina, A. Disease resistance or growth: the role of plant hormones in balancing immune responses and fitness costs. Front. Plant Sci. 4, https://doi.org/10.3389/fpls.2013.00155 (2013).
Tzin, V. & Galili, G. The biosynthetic pathways for shikimate and aromatic amino acids in Arabidopsis thaliana. The Arabidopsis Book 8, e0132. 10.1199/tab.0132 (American Society of Plant Biologists, 2010).
Ishihara, A. et al. The tryptophan pathway is involved in the defense responses of rice against pathogenic infection via serotonin production. Plant J. 54, 481–495 (2008).
pubmed: 18266919
Hou, C. & Forman, R. Growth inhibition of plant pathogenic fungi by hydroxy fatty acids. J. Ind. Microbiol. Biotechnol. 24, 275–276 (2000).
Kachroo, A. & Kachroo, P. Fatty acid–derived signals in plant defense. Annu. Rev. Phytopathol. 47, 153–176 (2009).
pubmed: 19400642
Prost, I. Evaluation of the antimicrobial activities of plant oxylipins supports their involvement in defense against pathogens. Plant Physiol. 139, 1902–1913 (2005).
pubmed: 16299186
pmcid: 1310568
Lim, G. H., Singhal, R., Kachroo, A. & Kachroo, P. Fatty acid– and lipid-mediated signaling in plant defense. Annu. Rev. Phytopathol. 55, 505–36 (2017).
pubmed: 28777926
Göbel, C., Feussner, I., Hamberg, M. & Rosahl, S. Oxylipin profiling in pathogen-infected potato leaves. Biochim. Biophys. Acta (Mol. Cell. Biol. Lipids) 1584, 55–64 (2002).
Walters, D. R., Cowley, T. & Weber, H. Rapid accumulation of trihydroxy oxylipins and resistance to the bean rust pathogen Uromyces fabae following wounding in Vicia faba. Ann. Bot. 97, 779–784 (2006).
pubmed: 16492683
pmcid: 2803428
Gamir, J., Pastor, V., Kaever, A., Cerezo, M. & Flors, V. Targeting novel chemical and constitutive primed metabolites against Plectosphaerella cucumerina. Plant J. 78, 227–240 (2014).
pubmed: 24506441
Ngara, R. et al. Identifying differentially expressed proteins in sorghum cell cultures exposed to osmotic stress. Sci. Rep. 8, https://doi.org/10.1038/s41598-018-27003-1 (2018).
Goossens, A., Häkkinen, S., Laakso, I., Oksman-Caldentey, K. & Inzé, D. Secretion of secondary metabolites by ATP-binding cassette transporters in plant cell suspension cultures. Plant Physiol. 131, 1161–1164 (2003).
pubmed: 12644666
pmcid: 1540296
Shitan, N. Secondary metabolites in plants: Transport and self-tolerance mechanisms. Biosci. Biotechnol. Biochem. 80, 1283–1293 (2016).
pubmed: 26940949
Yogendra, K. N. et al. Quantitative resistance in potato leaves to late blight associated with induced hydroxycinnamic acid amides. Funct. Integr. Genom. 14, 285–298 (2014).
Gauthier, L., Atanasova-Penichon, V., Chéreau, S. & Richard-Forget, F. Metabolomics to decipher the chemical defense of cereals against Fusarium graminearum and deoxynivalenol accumulation. Int. J. Mol. Sci. 16, 24839–24872 (2009).
Naoumkina., M. A. et al. Genome-wide analysis of phenylpropanoid defence pathways. Mol. Plant Pathol. 11, 829–846 (2010).
pubmed: 21029326
pmcid: 6640277
Balmer, D., De Papajewski, D. V., Planchamp, C., Glauser, G. & Mauch-Mani, B. Induced resistance in maize is based on organ-specific defence responses. Plant J. 74, 213–225 (2013).
pubmed: 23302050
Kumar, S. & Pandey, A. Chemistry and biological activities of flavonoids: An overview. Sci. World J. Article ID 162750, https://doi.org/10.1155/2013/162750 (2013).
Wang, Y., Chantreau, M., Sibout, R. & Hawkins, S. Plant cell wall lignification and monolignol metabolism. Front. Plant Sci. 4, 1–14 (2013).
Pushpa, D., Yogendra, K. N., Gunnaiah, R., Kushalappa, A. C. & Murphy, A. Identification of late blight resistance-related metabolites and genes in potato through nontargeted metabolomics. Plant Mol. Biol. Report. 32, 584–595 (2014).
Gunnaiah, R. & Kushalappa, A. C. Metabolomics deciphers the host resistance mechanisms in wheat cultivar Sumai-3, against trichothecene producing and non-producing isolates of Fusarium graminearum. Plant Physiol. Biochem. 83, 40–50 (2014).
pubmed: 25084325
Cuperlovic-Culf, M., Rajagopalan, N., Tulpan, D. & Loewen, M.C. Metabolomics and cheminformatics analysis of antifungal function of plant metabolites. Metabolites, 6, https://doi.org/10.3390/metabo6040031 (2016).
Taheri, P. & Tarighi, S. A survey on basal resistance and riboflavin-induced defense responses of sugar beet against Rhizoctonia solani. J. Plant Physiol. 168, 1114–1122 (2011).
pubmed: 21269732
Gerber, I. B., Zeidler, D., Durner, J. & Dubery, I. A. Early perception responses of Nicotiana tabacum cells in response to lipopolysaccharides from Burkholderia cepacia. Planta 218, 647–657 (2004).
pubmed: 14605884
De Castro, C., Parrilli, M., Holst, O. & Molinaro, A. Microbe-associated molecular patterns in innate immunity. Extraction and chemical analysis of Gram-negative bacterial lipopolysaccharides. Methods Enzymol. 480, 89–115 (2010).
pubmed: 20816206
Coventry, H. S. & Dubery, I. A. Lipopolysaccharides from Burkholderia cepacia contribute to an enhanced defensive capacity and the induction of pathogenesis-related proteins in Nicotiana tabacum. Physiol. Mol. Plant Pathol. 58, 149–158 (2001).
Leontein, K. Assignment of absolute configuration of sugars by glc of their acetylated glycosides formed from chiral alcohols. Meth. Carbohydr. Chem. 62, 359–362 (1978).
Ciucanu, I. & Kerek, F. A simple and rapid method for the permethylation of carbohydrates. Carbohydr Res. 131, 209–217 (1984).
Rietschel, E. Absolute configuration of 3-hydroxy fatty acids present in lipopolysaccharides from various bacterial groups. Eur. J. Biochem. 64, 423–428 (1976).
pubmed: 1278168
Bligh, E. G. & Dyer, W. J. A rapid method for total lipid extraction and purification. Can. J. Biochem. Physiol. 37, 911–917 (1959).
pubmed: 13671378
Piantini, U., Sorensen, O. W. & Ernst, R. R. Multiple quantum filters for elucidating NMR coupling networks. J. Am. Chem. Soc. 104, 6800–6801 (1982).
Rance., M. et al. Improved spectral resolution in COSY (1)H NMR spectra of proteins via double quantum filtering. Biochem. Biophys. Res. Commun. 425, 527–533 (1983).
States, D. J., Haberkorn, R. A. & Ruben, D. A two-dimensional nuclear Overhauser experiment with pure absorption phase in four quadrants. J. Magn. Res. 8, 286–292 (1982).
Stern, A. S., Li, K. B. & Hoch, J. C. Modern spectrum analysis in multidimensional NMR spectroscopy: comparison of linear-prediction extrapolation and maximum-entropy reconstruction. J. Am. Chem. Soc. 124, 1982–1993 (2002).
pubmed: 11866612
Silipo, A. et al. Structure elucidation of the highly heterogeneous lipid A from the lipopolysaccharide of the Gram-negative extremophile bacterium Halomonas magadiensis Strain 21 M1. Eur. J. Org. Chem. 10, 2263–2271 (2004).
Sturiale, L. et al. Reflectron MALDI TOF and MALDI TOF/TOF mass spectrometry reveal novel structural details of native lipooligosaccharides. J. Mass Spectrom. 46, 1135–1142 (2011).
pubmed: 22124985
Murashige, T. & Skoog, F. A revised medium for rapid growth and bioassays with tobacco tissue cultures. Physiol. Plant. 15, 473–497 (1962).
Madala, N. E., Steenkamp, P. A., Piater, L. A. & Dubery, I. A. Different metabolite distribution patterns in isonitrosoacetophenone elicited tobacco and sorghum cells as revealed by multivariate statistical models. Springer Plus Online 3, 254, https://doi.org/10.1186/2193-1801-3-25 (2014).
doi: 10.1186/2193-1801-3-25
Kang, J., Price, W. E., Ashton, J., Tapsell, L. C. & Johnson, S. Identification and characterization of phenolic compounds in hydromethanolic extracts of sorghum wholegrains by LC-ESI-MS
pubmed: 27283625